Advertisement

Intestinal Trematode Infections

  • Rafael Toledo
  • Carla Muñoz-Antoli
  • J. Guillermo Esteban
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 766)

Abstract

Intestinal trematodes are among the most common types of parasitic worms. About 76 species belonging to 14 families have been recorded infecting humans. Infection commonly occurs when humans eat raw or undercooked foods that contain the infective metacercariae. These parasites are diverse in regard to their morphology, geographical distribution and life cycle, which make it difficult to study the parasitic diseases that they cause. Many of these intestinal trematodes have been considered as endemic parasites in the past. However, the geographical limits and the population at risk are currently expanding and changing in relation to factors such as growing international markets, improved transportation systems, new eating habits in developed countries and demographic changes. These factors make it necessary to better understand intestinal trematode infections. This chapter describes the main features of human intestinal trematodes in relation to their biology, epidemiology, host–parasite relationships, pathogenicity, clinical aspects, diagnosis, treatment and control.

Keywords

Intermediate Host Adult Worm Definitive Host Ventral Sucker Heavy Infection 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgment

This work was supported by the projects PROMETEO/2009/081 from Conselleria d’Educació, Generalitat Valenciana (Valencia, Spain).

References

  1. 1.
    Fürst T, Keiser J, Utzinger J (2012) Global burden of human food-borne trematodiasis: a systematic review and meta-analysis. Lancet Infect Dis 12:210–221PubMedGoogle Scholar
  2. 2.
    Gibson DI, Bray RA (1994) The evolutionary expansion and host-parasite relationship of the Digenea. Int J Parasitol 24:1213–1226PubMedGoogle Scholar
  3. 3.
    Yamaguti S (1975) A synoptical review of the life histories of digenetic trematodes of vertebrates: with special reference to the morphology of their larval forms. Keigaku, TokyoGoogle Scholar
  4. 4.
    Butcher AR, Talbot GA, Norton RE et al (1996) Locally acquired Brachylaima sp. (Digenea: Brachylaimidae) intestinal fluke infection in two South Australian infants. Med J Aust 164:475–478PubMedGoogle Scholar
  5. 5.
    Butcher AR, Parasuramar PS, Thompson CS et al (1998) First report of the isolation of an adult worm of the genus Brachylaima (Digenea: Brachylaimidae), from the gastrointestinal tract of a human. Int J Parasitol 28:607–610PubMedGoogle Scholar
  6. 6.
    Butcher AR, Grove DI (2001) Description of the life-cycle stages of Brachylaima cribbi n. sp. (Digenea: Brachylaimidae) derived from eggs recovered from human faeces in Australia. Syst Parasitol 49:211–221PubMedGoogle Scholar
  7. 7.
    Butcher AR, Palethorpe HM, Grove DI (2002) Effects of sex and age on the susceptibility of C57BL/6J mice to infection with Brachylaima cribbi and the course of the infection in NOD SCID mice. Parasitol Res 88:668–674PubMedGoogle Scholar
  8. 8.
    Butcher AR, Palethorpe HM, Grove DI (2003) Response to re-infection with Brachylaima cribbi in immunocompetent and immunodeficient mice. Parasitol Int 52:219–228PubMedGoogle Scholar
  9. 9.
    Niewiadomska K (2002) Family Diplostomidae Poirier, 1886. In: Gibson DI, Jones A, Bray RA (eds) Keys to the Trematoda, vol 1. CABI, WallingfordGoogle Scholar
  10. 10.
    Hong ST, Hong SJ, Lee SH et al (1982) Studies on Intestinal trematodes in Korea: VI. On the metacercaria and the second intermediate host of Fibricola seoulensis. Korean J Parasitol 20:101–111Google Scholar
  11. 11.
    Cribb TH, Bray RA, Olson PD et al (2003) Life cycle evolution in the Digenea: a new perspective from phylogeny. Adv Parasitol 54:197–254PubMedGoogle Scholar
  12. 12.
    Fried B, Graczyk TK, Tamang L (2004) Food-borne intestinal trematodiases in humans. Parasitol Res 93:159–170PubMedGoogle Scholar
  13. 13.
    Shoop WL (1989) Experimental human infection with Fibricola cratera (Trematoda: Neodiplostomidae). Korean J Parasitol 27:249–252Google Scholar
  14. 14.
    Chai JY, Lee SH (1991) Intestinal trematodes infecting humans in Korea. Southeast Asian J Trop Med Public Health 22:163–170PubMedGoogle Scholar
  15. 15.
    Chai JY, Lee SH (2002) Food-borne intestinal trematode infections in the Republic of Korea. Parasitol Int 51:129–154PubMedGoogle Scholar
  16. 16.
    Seo BS, Rim HJ, Lee CW (1964) Studies on the parasitic helmiths of Korea: I. Trematodes of rodents. Korean J Parasitol 2:20–26Google Scholar
  17. 17.
    Seo BS, Lee SH, Chai JY et al (1988) The life cycle and larval development of Fibricola seoulensis (Trematoda: Diplostomatidae). Korean J Parasitol 26:179–188Google Scholar
  18. 18.
    Chai JY, Shin EH, Lee SH et al (2009) Foodborne intestinal flukes in Southeast Asia. Korean J Parasitol 47:S69–S102PubMedCentralPubMedGoogle Scholar
  19. 19.
    Chung PR, Jung Y, Kim DS (1996) Segmentina (Polypylis) hemisphaerula (Gastropoda: Planorbidae): a new molluscan intermediate host of a human intestinal fluke Neodiplostomum seoulensis (Trematoda: Diplostomatidae) in Korea. J Parasitol 82:336–338PubMedGoogle Scholar
  20. 20.
    Chung PR, Jung Y, Park YK et al (2002) Host specificity of Austropeplea ollula (Gastropoda: Lymnaeidae) to miracidial infection with a human intestinal fluke Neodiplostomum seoulense (Trematoda: Diplostomatidae) in Korea. J Parasitol 88:630–631PubMedGoogle Scholar
  21. 21.
    Hong SJ, Lee SH, Seo BS et al (1983) Studies on intestinal trematodes in Korea: IX. Recovery rate and development of Fibricola seoulensis in experimental animals. Korean J Parasitol 21:224–233Google Scholar
  22. 22.
    Seo BS, Lee SH, Hong ST et al (1982) Studies on intestinal trematodes in Korea: V. A human case infected by Fibricola seoulensis (Trematoda: Diplostomatidae). Korean J Parasitol 20:93–99Google Scholar
  23. 23.
    Hong ST, Chai JY, Lee SH (1984) Ten human cases of Fibricola seoulensis infection and mixed one with Stellantchasmus and Metagonimus. Korean J Parasitol 24:95–97Google Scholar
  24. 24.
    Hong ST, Cho TK, Hong SJ et al (1984) Fifteen human cases of Fibricola seoulensis infection in Korea. Korean J Parasitol 22:61–65Google Scholar
  25. 25.
    Toledo R, Esteban JG, Fried B (2006) Immunology and pathology of intestinal trematodes in their definitive hosts. Adv Parasitol 63:285–365PubMedGoogle Scholar
  26. 26.
    Huh S, Chai JY, Hong ST et al (1988) Clinical and histopathological findings in mice heavily infected with Fibricola seoulensis. Korean J Parasitol 26:45–53Google Scholar
  27. 27.
    Kook J, Nawa Y, Lee SH et al (1998) Pathogenicity and lethality of a minute intestinal fluke, Neodiplostomum seoulense, to various strains of mice. J Parasitol 84:1178–1183PubMedGoogle Scholar
  28. 28.
    Lee SH, Yoo BH, Hong ST et al (1985) A histopathological study on the intestine of mice and rats experimentally infected by Fibricola seoulensis. Korean J Parasitol 23:58–72Google Scholar
  29. 29.
    Huh S, Lee SH, Seo BS (1990) Histochemical findings of the tribocytic organ and tegument of Fibricola seoulensis. Korean J Parasitol 28:155–160Google Scholar
  30. 30.
    Huh S, Hong ST (1993) Transmission electron microscopic findings of the tribocytic organ of Fibricola seoulensis. Korean J Parasitol 31:315–320PubMedGoogle Scholar
  31. 31.
    Pyo KH, Kang EY, Jung BK et al (2012) Depressed neuronal growth associated protein (GAP)-43 expression in the small intestines of mice experimentally infected with Neodiplostomum seoulense. Korean J Parasitol 50:89–93PubMedCentralPubMedGoogle Scholar
  32. 32.
    Yu JR, Hong ST, Chai JY et al (1995) The effect of reinfection with Neodiplostomum seoulensis on the histopathology and activities of brush border membrane bound enzymes in the rat small intestine. Korean J Parasitol 33:37–43PubMedGoogle Scholar
  33. 33.
    Chai JY, Kim TK, Cho WH et al (1998) Intestinal mastocytosis and goblet cell hyperplasia in BALB/c and C3H mice infected with Neodiplostomum seoulense. Korean J Parasitol 36:109–119PubMedGoogle Scholar
  34. 34.
    Shin EH, Kim TH, Hong SJ et al (2003) Effects of anti-allergic drugs on intestinal mastocytosis and worm expulsion of rats infected with Neodiplostomum seoulense. Korean J Parasitol 41:81–87PubMedCentralPubMedGoogle Scholar
  35. 35.
    Shin EH, Lee SH, Kim JL et al (2007) T-helper-1 and T-helper-2 immune responses in mice infected with the intestinal fluke Neodiplostomum seoulense: their possible roles in worm expulsion and host fatality. J Parasitol 93:1036–1045PubMedGoogle Scholar
  36. 36.
    Han ET, Chen JH, Chai JY (2008) Antibody responses in sera of different mouse strains experimentally infected with Neodiplostomum seoulense. Korean J Parasitol 46:279–283PubMedCentralPubMedGoogle Scholar
  37. 37.
    Lee JC, Kong Y, Lee SU et al (1997) Localization of worm antigen in Neodiplostomum seoulense by immuno-electronmicroscopy. Korean J Parasitol 35:95–104PubMedGoogle Scholar
  38. 38.
    Kim TY, Han KY, Shin EH et al (2008) Antigenic properties of cystatin-binding cysteine proteinases from Neodiplostomum seoulense. J Parasitol 94:654–658PubMedGoogle Scholar
  39. 39.
    Toledo R, Esteban JG, Fried B (2009) Recent advances in the biology of echinostomes. Adv Parasitol 69:147–204PubMedGoogle Scholar
  40. 40.
    Kostadinova A, Gibson DI (2000) The systematics of the Echinostomes. In: Fried B, Graczyk TK (eds) Echinostomes as experimental models for biological research. Kluwer, DordrechtGoogle Scholar
  41. 41.
    Fried B, Toledo R (2004) Criteria for species determination in the “revolutum” group of Echinostoma. J Parasitol 90:917PubMedGoogle Scholar
  42. 42.
    Kostadinova A (2005) Family Echinostomatidae Looss, 1899. In: Gibson DI, Jones A, Bray RA (eds) Keys to the Trematoda, vol 2. CABI, WallingfordGoogle Scholar
  43. 43.
    Esteban JG, Muñoz-Antoli C (2009) Echinostomes: Systematics and life cycles. In: Fried B, Toledo R (eds) The biology of Echinostomes. From the molecule to the community. Springer, New YorkGoogle Scholar
  44. 44.
    Graczyk TK, Fried B (1998) Echinostomiasis: a common but forgotten food-borne disease. Am J Trop Med Hyg 58:501–504PubMedGoogle Scholar
  45. 45.
    Belizario VY, Geronilla GG, Anastacio MBM et al (2007) Echinostoma malayanum infection, in the Philippines. Emerg Infect Dis 13:1130–1131PubMedCentralPubMedGoogle Scholar
  46. 46.
    Sohn WM, Kim HJ, Yong TS et al (2011) Echinostoma ilocanum infection in Oddar Meanchey Province, Cambodia. Korean J Parasitol 49:187–190PubMedCentralPubMedGoogle Scholar
  47. 47.
    Sohn WM, Chai JY, Yong TS et al (2011) Echinostoma revolutum infection in children, Pursat Province, Cambodia. Emerg Infect Dis 17:117–119PubMedCentralPubMedGoogle Scholar
  48. 48.
    Xiao X, Dabing L, Tianping W et al (1995) Studies on mode of human infection with Echinochasmus liliputanus. Chinese J Parasitol Parasit Dis 13:197–199Google Scholar
  49. 49.
    Tantrawatpan C, Saijuntha W, Sithithaworn P et al (2013) Genetic differentiation of Artyfechinostomum malayanum and A. sufrartyfex (Trematoda: Echinostomatidae) based on internal transcribed spacer sequences. Parasitol Res 112:437–441PubMedGoogle Scholar
  50. 50.
    Haseeb MA, Eveland LK (2000) Human echinostomiasis: mechanisms of pathogenesis and host resistance. In: Fried B, Graczyk TK (eds) Echinostomes as experimental models for biological research. Kluwer, DordrechtGoogle Scholar
  51. 51.
    Chai JY (2007) Intestinal flukes. In: Murrell KD, Fried B (eds) Food-borne parasitic zoonoses: fish and plant-borne parasites, world class parasites, vol 11. Springer, New YorkGoogle Scholar
  52. 52.
    Chai JY (2009) Echinostomes in humans. In: Fried B, Toledo R (eds) The biology of Echinostomes. From the molecule to the community. Springer, New YorkGoogle Scholar
  53. 53.
    Cheng YZ, Lin JX, Fang YY et al (1992) Discovery of human infection with Echinostoma angustitestis. Chin J Zoonoses 8:7–8Google Scholar
  54. 54.
    Yu S, Mott K (1994) Epidemiology and morbidity of food-borne intestinal trematode infections. Trop Dis Bull 91:R125–R152Google Scholar
  55. 55.
    Xiao X, Wang TP, Lu DB et al (1992) The first record of human infection with Echinochasmus liliputanus. Chinese J Parasitol Parasit Dis 10:132–135Google Scholar
  56. 56.
    Liang C, Ke XL (1988) Echinochasmus jiufoensis sp. nov., a human parasite from Guangzhou (Trematoda: Echinostomatidae). Acta Zootax Sinica 13:4–8Google Scholar
  57. 57.
    Chen XQ, Feng GX, Qian ZF (1993) Survey on infection due to Echinostoma hortense in Liaoning Province. Chinese J Parasitol Parasit Dis 11:226Google Scholar
  58. 58.
    Carney WP, Sudomo M, Purnomo A (1980) Echinostomiasis: a disease that disappeared. Trop Geograph Med 32:101–105Google Scholar
  59. 59.
    Clarke MD, Carney WP, Cross JH et al (1974) Schistosomiasis and other human parasitoses of Lake Lindu in Central Sulawesi (Celebes), Indonesia. Am J Trop Med Hyg 23:385–392PubMedGoogle Scholar
  60. 60.
    Kusharyono C, Sukartinah S (1991) The current status of foodborne parasitic zoonoses in Indonesia. Southeast Asian J Trop Med Public Health 22:8–10PubMedGoogle Scholar
  61. 61.
    Cross JH, Clarke MD, Cole WC (1976) Parasitic infection in humans in West Kalimantan (Borneo) Indonesia. Trop Geograph Med 28:121–130Google Scholar
  62. 62.
    Sayasone S, Mak TK, Vanmany M et al (2011) Helminth and intestinal protozoa infections, multiparasitism and risk factors in Champasack province, Lao People’s Democratic Republic. PLoS Negl Trop Dis 5:e1037PubMedCentralPubMedGoogle Scholar
  63. 63.
    Majima M (1927) On Echinostoma macrorchis found in man. Kumamoto Igakkai Zasshi 2252:2260Google Scholar
  64. 64.
    Hirazawa I (1928) On Echinochasmus perfoliatus (Ratz) found in man. Tokyo Iji Shinshi 2577:1328–1334Google Scholar
  65. 65.
    Radomyos P, Bunnag D, Harinasuta T (1985) Report of Episthmium caninum (Verma, 1935) Yamaguti, 1958 (Digenea: Echinostomatidae) in man. Southeast Asian J Trop Med Public Health 16:508–511PubMedGoogle Scholar
  66. 66.
    Radomyos P, Charoenlarp P, Harinasuta T (1991) Human Episthmium caninum (Digenea: Echinostomatidae) infection: report of two more cases. J Trop Med Parasitol 14:48–50Google Scholar
  67. 67.
    Bandyopadhyay AK, Nandy A (1986) A preliminary observation on the prevalence of echinostomes in a tribal community near Calcutta. Ann Trop Med Parasitol 80:373–375PubMedGoogle Scholar
  68. 68.
    Bandyopadhyay AK, Manna B, Nandy A (1989) Human infection of Artyfechinostomum oraoni n. sp. (Paryphostominae: Echinostomatidae) in a tribal community, “Oraons” in West Bengal, India. Indian J Parasitol 13:191–196Google Scholar
  69. 69.
    Takahashi S, Ishii T, Ueno N (1930) A human case of Echinostoma cinetorchis. Tokyo Iji Shinshi 2757:141–144Google Scholar
  70. 70.
    Kawahara S, Yamamoto E (1933) Human cases of Echinostoma cinetorchis. Tokyo Iji Shinshi 2840:1794–1796Google Scholar
  71. 71.
    Seo ES, Cho SY, Chai JY (1980) Studies on intestinal trematodes in Korea. I. A human case of Echinostoma cinetorchis infection with an epidemiological investigation. Seoul J Med 21:21–29Google Scholar
  72. 72.
    Ryang YS, Ahn YK, Kim WT et al (1986) Two cases of human infection by Echinostoma cinetorchis. Korean J Parasitol 24:71–76Google Scholar
  73. 73.
    Lee SK, Chung NS, Ko IH (1988) An epidemiological survey of Echinostoma hortense infection in Chongsong-gun, Kyongbuk Province. Korean J Parasitol 26:199–206Google Scholar
  74. 74.
    Yokogawa M, Harinasutam C, Charoenlarp P (1965) Hypoderaeum conoideum (Block, 1782) Diez, 1909, a common intestinal fluke of man in the north-east Thailand. Japanese J Parasitol 14:148–153Google Scholar
  75. 75.
    Chai JY, Sohn WM, Yong TS et al (2012) Echinostome flukes recovered from humans in Khammouane Province, Lao PDR. Korean J Parasitol 50:269–272PubMedCentralPubMedGoogle Scholar
  76. 76.
    Sayasone S, Tesana S, Utzinger J et al (2009) Rare human infection with the trematode Echinochasmus japonicus in Lao PDR. Parasitol Int 58:106–109PubMedGoogle Scholar
  77. 77.
    Lu SC (1982) Echinostomiasis in Taiwan. Int J Zoonoses 9:33–38PubMedGoogle Scholar
  78. 78.
    Carney WP (1991) Echinostomiasis –a snail-borne intestinal disease. Southeast Asian J Trop Med Public Health 22:206–211PubMedGoogle Scholar
  79. 79.
    Eduardo SL (1991) Food-borne zoonoses in the Philippines. Southeast Asian J Trop Med Public Health 22:16–22PubMedGoogle Scholar
  80. 80.
    Beaver PC, Jung RC, Cupp EW (1984) Clinical parasitology, 9th edn. Lea & Febiger, PhiladelphiaGoogle Scholar
  81. 81.
    DeGirolami PC, Kimber J (1983) Intestinal parasites among Southeast Asian refugees in Massachusetts. Am J Clin Pathol 79:502–504PubMedGoogle Scholar
  82. 82.
    Poland GA, Navin TR, Sarosi GA (1985) Outbreak of parasitic gastroenteritis among travelers returning from Africa. Arch Intern Med 145:2220–2221PubMedGoogle Scholar
  83. 83.
    Lee SK, Chung NS, Ko IH et al (1986) Two cases of natural human infection by Echinostoma hortense. Korean J Parasitol 24:77–81Google Scholar
  84. 84.
    Chai JY, Hong ST, Lee SH et al (1994) A case of echinostomiasis with ulcerative lesions in the duodenum. Korean J Parasitol 32:201–204PubMedGoogle Scholar
  85. 85.
    Chang YD, Sohn WM, Ryu JH et al (2005) A human infection of Echinostoma hortense in duodenal bulb diagnosed by endoscopy. Korean J Parasitol 43:57–60PubMedCentralPubMedGoogle Scholar
  86. 86.
    Park CJ, Kim J (2006) A human case of Echinostoma hortense infection diagnosed by endoscopy in area of southwestern Korea. Korean J Med 71:229–234Google Scholar
  87. 87.
    Cho CM, Tak WY, Kweon YO et al (2003) A human case of Echinostoma hortense (Trematoda: Echinostomatidae) infection diagnosed by gastroduodenal endoscopy in Korea. Korean J Parasitol 41:117–120PubMedCentralPubMedGoogle Scholar
  88. 88.
    Huffman JE, Iglesias D, Fried B (1988) Echinostoma revolutum: pathology of extraintestinal infection in the golden hamster. Int J Parasitol 18:873–874PubMedGoogle Scholar
  89. 89.
    Mabus J, Huffman JE, Fried B (1988) Humoral and cellular response to infection with Echinostoma revolutum in the golden hamster, Mesocricetus auratus. J Helminthol 62:127–132PubMedGoogle Scholar
  90. 90.
    Toledo R, Monteagudo C, Espert A et al (2006) Echinostoma caproni: intestinal pathology in the golden hamster, a highly compatible host, and the Wistar rat, a less compatible host. Exp Parasitol 112:164–171PubMedGoogle Scholar
  91. 91.
    Muñoz-Antoli C, Sotillo J, Monteagudo C et al (2007) Development and pathology of Echinostoma caproni in experimentally infected mice. J Parasitol 93:854–859PubMedGoogle Scholar
  92. 92.
    Fujino T, Fried B (1996) The expulsion of Echinostoma trivolvis from C3H mice: differences in glycoconjugates in mouse versus hamster small intestinal mucosa during infection. J Helminthol 70:115–121PubMedGoogle Scholar
  93. 93.
    Weinstein MS, Fried B (1991) The expulsion of Echinostoma trivolvis and retention of Echinostoma caproni in the ICR mouse: pathological effects. Int J Parasitol 21:255–257PubMedGoogle Scholar
  94. 94.
    Toledo R, Fried B (2005) Echinostomes as experimental models for interactions between adult parasites and vertebrate hosts. Trends Parasitol 21:251–254PubMedGoogle Scholar
  95. 95.
    Toledo R (2009) Immunology and pathology of echinostomes in the definitive host. In: Fried B, Toledo R (eds) The biology of Echinostomes. From the molecule to the community. Springer, New YorkGoogle Scholar
  96. 96.
    Fujino T, Fried B, Tada I (1993) The expulsion of Echinostoma trivolvis: worm kinetics and intestinal cytopathology in conventional and congenitally athymic BALB/c mice. Parasitology 106:297–304PubMedGoogle Scholar
  97. 97.
    Fujino T, Fried B, Ichikawa H et al (1996) Rapid expulsion of the intestinal trematodes Echinostoma trivolvis and E. caproni from C3H mice by trapping with increased goblet cell mucins. Int J Parasitol 26:319–324PubMedGoogle Scholar
  98. 98.
    Fujino T, Ichikawa H, Fried B et al (1996) The expulsion of Echinostoma trivolvis: suppressive effects of dexamethasone on goblet cell hyperplasia and worm rejection in C3H/HeN mice. Parasite 3:283–289PubMedGoogle Scholar
  99. 99.
    Fujino T, Fried B (1993) Expulsion of Echinostoma trivolvis (Cort, 1914) Kanev, 1985 and retention of E. caproni Richard, 1964 (Trematoda, Echinostomatidae) in C3H mice: pathological, ultrastructural, and cytochemical effects on the host intestine. Parasitol Res 79:286–292PubMedGoogle Scholar
  100. 100.
    Kim I, Im JA, Lee KJ et al (2000) Mucosal mast cell responses in the small intestine of rats infected with Echinostoma hortense. Korean J Parasitol 38:139–143PubMedCentralPubMedGoogle Scholar
  101. 101.
    Park KY, Lee KJ, Kim IS et al (2005) Reaction of mast cells and goblet cells in the small intestine of C57BL/6 and C3H/HeN mice infected with Echinostoma hortense. Korean J Biomed Lab Sci 11:259–266Google Scholar
  102. 102.
    Ryang YS, Yang EJ, Kim JL et al (2007) Immune response and inhibitory effect of ketotifen on the BALB/c and C3H/HeN mice infected with Echinostoma hortense. Parasitol Res 101:1103–1110PubMedGoogle Scholar
  103. 103.
    Graczyk TK, Fried B (1994) ELISA method for detecting anti-Echinostoma caproni (Trematoda: Echinostomatidae) immunoglobulins in experimentally infected ICR mice. J Parasitol 80:544–549PubMedGoogle Scholar
  104. 104.
    Toledo R, Espert A, Muñoz-Antoli C et al (2004) Kinetics of Echinostoma caproni (Trematoda: Echinostomatidae) antigens in feces and serum of experimentally infected hamsters and rats. J Parasitol 90:752–758PubMedGoogle Scholar
  105. 105.
    Sotillo J, Muñoz-Antoli C, Marcilla A et al (2007) Echinostoma caproni: Kinetics of IgM, IgA and IgG subclasses in the serum and intestine of experimentally infected rats and mice. Exp Parasitol 116:390–398PubMedGoogle Scholar
  106. 106.
    Cho YK, Ryang YS, Kim IS et al (2007) Differential immune profiles following experimental Echinostoma hortense infection in BALB/c and C3H/HeN mice. Parasitol Res 100:1053–1061PubMedGoogle Scholar
  107. 107.
    Sotillo J, Valero L, Sánchez del Pino MM et al (2008) Identification of antigenic proteins from Echinostoma caproni (Trematoda: Echinostomatidae) recognized by mouse immunoglobulins M, A and G using an immunoproteomic approach. Parasite Immunol 30:271–279PubMedGoogle Scholar
  108. 108.
    Lee KJ, Jin D, Chang BS et al (2009) The immunological effects of electrolyzed reduced water on the Echinostoma hortense infection in C57BL/6 mice. Biol Pharm Bull 32:456–462PubMedGoogle Scholar
  109. 109.
    Brunet LR, Joseph S, Dunne DW et al (2000) Immune responses during the acute stages of infection with the intestinal trematode Echinostoma caproni. Parasitology 120:565–571PubMedGoogle Scholar
  110. 110.
    Sotillo J, Trelis M, Cortes A et al (2011) Th17 responses in Echinostoma caproni infections in hosts of high and low compatibility. Exp Parasitol 129:307–311PubMedGoogle Scholar
  111. 111.
    Trelis M, Sotillo J, Monteagudo C et al (2011) Echinostoma caproni (Trematoda): differential in vivo cytokine responses in high and low compatible hosts. Exp Parasitol 127:387–397PubMedGoogle Scholar
  112. 112.
    Agger MK, Simonsen PE, Vennervald BJ (1993) The antibody response in serum, intestinal wall and intestinal lumen of NMRI mice infected with Echinostoma caproni. J Helminthol 67:169–178PubMedGoogle Scholar
  113. 113.
    Graczyk TK, Fried B (1995) An enzyme-linked immunosorbent assay for detecting anti-Echinostomatrivolvis (Trematoda) IgG in experimentally infected ICR mice. Cross-reactivity with E. caproni. Parasitol Res 81:710–712Google Scholar
  114. 114.
    Toledo R, Espert A, Muñoz-Antoli C et al (2003) Development of an antibody-based capture enzyme-linked immunosorbent assay for detecting Echinostoma caproni (Trematoda) in experimentally infected rats: kinetics of coproantigen excretion. J Parasitol 89:1227–1231PubMedGoogle Scholar
  115. 115.
    Toledo R, Espert A, Muñoz-Antoli C et al (2005) Kinetics of antibodies and antigens in serum of mice experimentally infected with Echinostoma caproni (Trematoda: Echinostomatidae). J Parasitol 91:978–980PubMedGoogle Scholar
  116. 116.
    Mas-Coma S, Bargues MD, Valero MA (2005) Fascioliasis and other plant-borne trematode zoonoses. Int J Parasitol 35:1255–1278PubMedGoogle Scholar
  117. 117.
    Gilman RH, Mondal G, Maskud M et al (1982) Endemic focus of Fasciolopsis buski in Bangladesh. Am J Trop Med Hyg 31:796–802PubMedGoogle Scholar
  118. 118.
    Weng YL, Zhuang ZL, Jiang HP et al (1989) Studies on ecology of Fasciolopsis buski and control strategy of fasciolopsiasis. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 7:108–111PubMedGoogle Scholar
  119. 119.
    Jaroonvesama N, Charoenlarp K, Areekul S (1986) Intestinal absorption studies in Fasciolopsis buski infection. Southeast Asian J Trop Med Public Health 17:582–586PubMedGoogle Scholar
  120. 120.
    Muttalib MA, Islam N (1975) Fasciolopsis buski in Bangladesh: a pilot study. J Trop Med Hyg 78:135–137PubMedGoogle Scholar
  121. 121.
    Rahman KM, Idris M, Khan AKA (1981) A study of fasciolopsiasis in Bangladesh. J Trop Med Hyg 84:81–86PubMedGoogle Scholar
  122. 122.
    Bunnag D, Radomyos P, Harinasuta T (1983) Field trial on the treatment of fasciolopsiasis with praziquantel. Southeast Asian J Trop Med Public Health 14:216–219PubMedGoogle Scholar
  123. 123.
    Shyu LY, Lee HH, Chen ER (1984) A preliminary study on epidemiology of fasciolopsiasis in Tainan Hsien, south Taiwan. Chinese J Microbiol Immunol 17:118–120Google Scholar
  124. 124.
    D’Souza PE, Jagannath MS, Prasanna KM (2001) A note on the occurrence of Fasciolopsis buski in pigs. Cheiron 30:178–179Google Scholar
  125. 125.
    Buckley JJC (1939) Observations on Gastrodiscoides hominis and Fasciolopsis buski in Assam. J Helminthol 17:1–12Google Scholar
  126. 126.
    Manning GS, Brockelman WY, Yiyant V (1971) An analysis of the prevalence of Fasciolopsis buski in central Thailand using catalytic models. Am J Epidemiol 93:354–360PubMedGoogle Scholar
  127. 127.
    Quang TD, Duong TH, Richard-Lenoble D et al (2008) Emergence in humans of fascioliasis (from Fasciola gigantica) and intestinal distomatosis (from Fasciolopsis buski) in Laos. Sante 18:119–124 (in French)PubMedGoogle Scholar
  128. 128.
    Bhattacharjee HK, Yadav D, Bagga D (2009) Fasciolopsis presenting as intestinal perforation: a case report. Tropical Gastroenterol 30:40–41Google Scholar
  129. 129.
    Mas-Coma S, Bargues MD, Valero MA (2006) Gastrodiscoidiasis, a plant-borne zoonotic disease caused by the intestinal amphistome fluke Gastrodiscoides hominis (Trematoda: Gastrodiscidae). Rev Iber Parasitol 66:75–81Google Scholar
  130. 130.
    Marty AM, Andersen EM (2000) Fasciolopsiasis and other intestinal trematodiasis. In: Neafie RC, Marty A, Wear DJ, Meyers WM (eds) Pathology of infectious diseases, vol I, Helminthiases. Armed Forces Institute of Pathology, American Registry of Pathology, Washington, DCGoogle Scholar
  131. 131.
    Cremonte F, Pina S, Gilardoni C et al (2013) A new species of gymnophallid (Digenea) and an amended diagnosis of the genus Gymnophalloides Fujita, 1925. J Parasitol 99:85–92PubMedGoogle Scholar
  132. 132.
    Toledo R, Esteban JG, Fried B (2012) Current status of food-borne trematode infections. Eur J Clin Microbiol Infect Dis 31:1705–1718PubMedGoogle Scholar
  133. 133.
    Lee SH, Chai JY, Hong ST (1993) Gymnophalloides seoi n. sp. (Digenea: Gymnophallidae), the first report of human infection by a gymnophallid. Korean J Parasitol 79:677–680Google Scholar
  134. 134.
    Chai JY, Choi MH, Yu JR et al (2003) Gymnophalloides seoi, a new human intestinal trematode. Trends Parasitol 19:109–112PubMedGoogle Scholar
  135. 135.
    Lee SH, Sohn WM, Hong SJ et al (1996) A nationwide survey of naturally produced oysters for infection with Gymnophalloides seoi metacercariae. Korean J Parasitol 34:107–112PubMedGoogle Scholar
  136. 136.
    Chai JY, Kim IM, Seo M et al (1997) A new focus of Heterophyes nocens, Pygidiopsis summa, and other intestinal flukes in a coastal area of Muan-gun, Chollanam-do. Korean J Parasitol 35:233–238PubMedGoogle Scholar
  137. 137.
    Chai JY, Han ET, Shin EH et al (2009) High prevalence of Haplorchis taichui, Phaneropsolus molenkampi, and other helminth infections among people in Khammouane province, Lao PDR. Korean J Parasitol 47:243–247PubMedCentralPubMedGoogle Scholar
  138. 138.
    Guk SM, Park JH, Shin EH et al (2006) Prevalence of Gymnophalloides seoi infection in coastal villages of Haenamgun and Yeongam-gun, Republic of Korea. Korean J Parasitol 44:1–5PubMedCentralPubMedGoogle Scholar
  139. 139.
    Cho SH, Cho PY, Lee DM et al (2010) Epidemiological survey on the infection of intestinal flukes in residents of Muan-gun, Jeollanam-do, the Republic of Korea. Korean J Parasitol 48:133–138PubMedCentralPubMedGoogle Scholar
  140. 140.
    Lee SH, Chai JY, Seo M et al (1995) Two cases of Gymnophalloides seoi infection accompanied by diabetes mellitus. Korean J Parasitol 33:61–64PubMedGoogle Scholar
  141. 141.
    Sohn WM, Ryang YS, Chai JY et al (1998) Discovery of Gymnophalloides seoi metacercariae in oysters from islands of the West Sea known as the habitats of paleartic oystercatchers. Korean J Parasitol 36:163–169PubMedCentralPubMedGoogle Scholar
  142. 142.
    Seo M, Chun H, Ahn G et al (2006) A case of colonic lymphoid tissue invasion by Gymnophalloides seoi in a Korean man. Korean J Parasitol 44:87–89PubMedCentralPubMedGoogle Scholar
  143. 143.
    Chai JY, Lee HS, Hong SJ et al (2001) Intestinal histopathology and in situ postures of Gymnophalloides seoi in experimentally infected mice. Korean J Parasitol 39:31–41PubMedCentralPubMedGoogle Scholar
  144. 144.
    Guk SM, Lee JH, Kim HJ et al (2009) CD4+ T-cell-dependent goblet cell proliferation and expulsion of Gymnophalloides seoi from the intestine of C57BL/6 mice. J Parasitol 95:581–590PubMedGoogle Scholar
  145. 145.
    Lee SH, Park SK, Seo M et al (1997) Susceptibility of various species of animals and strains of mice to Gymnophalloides seoi infection and the effects of immunosuppression in C3H/HeN mice. J Parasitol 83:883–886PubMedGoogle Scholar
  146. 146.
    Chai JY, Chung WJ, Kook J et al (1999) Growth and development of Gymnophalloides seoi in immunocompetent and immunosuppressed C3H/HeN mice. Korean J Parasitol 37:21–26PubMedCentralPubMedGoogle Scholar
  147. 147.
    Seo M, Guk SM, Han ET et al (2003) Role of intestinal goblet cells in the expulsion of Gymnophalloides seoi from mice. J Parasitol 89:1080–1082PubMedGoogle Scholar
  148. 148.
    Lee KD, Guk SM, Chai JY (2010) Toll-like receptor 2 and Muc2 expression on human intestinal epithelial cells by Gymnophalloides seoi adult antigen. J Parasitol 96:58–66PubMedGoogle Scholar
  149. 149.
    Lee JJ, Jung BK, Lim H et al (2012) Comparative morphology of minute intestinal fluke eggs that can occur in human stools in the Republic of Korea. Korean J Parasitol 50:207–213PubMedCentralPubMedGoogle Scholar
  150. 150.
    Yamaguti S (1971) Synopsis of digenetic trematodes of vertebrates. Keigaku, TokyoGoogle Scholar
  151. 151.
    Sohn WM (2009) Fish-borne zoonotic trematode metacercariae in the Republic of Korea. Korean J Parasitol 47:S103–S113PubMedCentralPubMedGoogle Scholar
  152. 152.
    Sheir ZM, Aboul-Enein ME (1970) Demographic, clinical and therapeutic appraisal of heterophyiasis. J Trop Med Hyg 73:148–152PubMedGoogle Scholar
  153. 153.
    Martínez-Alonso JC, Armentia A, Vega JM et al (1999) Anaphylactic reaction concurrent with Heterophyes heterophyes infestation. Rev Esp Alergol Inmunol Clin 14:37–39Google Scholar
  154. 154.
    Seo BS, Lee SH, Cho SY et al (1981) An epidemiologic study on clonorchiasis and metagonimiasis in riverside areas in Korea. Korean J Parasitol 19:137–150Google Scholar
  155. 155.
    Youn H (2009) Review of zoonotic parasites in medical and veterinary fields in the Republic of Korea. Korean J Parasitol 47:S133–S141PubMedCentralPubMedGoogle Scholar
  156. 156.
    Lee JJ, Kim HJ, Kim MJ et al (2008) Decrease of Metagonimus yokogawai endemicity along the Tamjin River basin. Korean J Parasitol 46:289–291PubMedCentralPubMedGoogle Scholar
  157. 157.
    Mahanta J, Narain K, Srivastava VK (1995) Heterophyid eggs in human stool samples in Assam: first report for India. J Commun Dis 27:142–145PubMedGoogle Scholar
  158. 158.
    Uppal B, Wadhwa V (2005) Rare case of Metagonimus yokogawai. Indian J Med Microbiol 23:61–62PubMedGoogle Scholar
  159. 159.
    Chai JY, Park JH, Han ET et al (2004) Prevalence of Heterophyes nocens and Pygydiopsis summa infections among residents in Western and Southern coastal islands of the Republic of Korea. Am J Trop Med Hyg 71:617–622PubMedGoogle Scholar
  160. 160.
    Chai JY, Huh S, Yu JR (1993) An epidemiological study of metagonimiasis along the upper reaches of the Namhau River. Korean J Parasitol 31:99–108PubMedGoogle Scholar
  161. 161.
    Eom KS, Son SY, Lee JS et al (1985) Heterophyid trematodes (Heterophyopsis continua, Pygidiopsis summa and Heterophyes heterophyes nocens) from domestic cats in Korea. Korean J Parasitol 23:197–202Google Scholar
  162. 162.
    Chung OS, Lee HJ, Kim YM et al (2011) First report of human infection with Gynaecotyla squatarolae and first Korean record of Haplorchis pumilio in a patient. Parasitol Int 60:227–229PubMedGoogle Scholar
  163. 163.
    Chai JY, Seo BS, Lee SH et al (1986) Human infections by Heterophyes heterophyes and H. dispar imported from Saudi Arabia. Korean J Parasitol 24:82–88Google Scholar
  164. 164.
    Trung Dung D, Van De N, Waikagul J et al (2007) Fishborne zoonotic intestinal trematodes, Vietnam. Emerg Infect Dis 13:1828–1833PubMedGoogle Scholar
  165. 165.
    Kino H, Suzuki Y, Oishi H et al (2006) Geographical distribution of Metagonimus yokogawai, and M. miyatai in Shizuoka Prefecture, Japan, and their site preferences in the sweetfish, Plecoglossus altivelis, and hamsters. Parasitol Int 55:201–206PubMedGoogle Scholar
  166. 166.
    Sayasone S, Vonghajack Y, Vanmany M et al (2009) Diversity of human intestinal helminthiasis in Lao PDR. Trans R Soc Trop Med Hyg 103:247–254PubMedGoogle Scholar
  167. 167.
    De NV, Le TH (2011) Human infections of fish-borne trematodes in Vietnam: prevalence and molecular specific identification at an endemic commune in Nam Dinh province. Exp Parasitol 129:355–361PubMedGoogle Scholar
  168. 168.
    Sripa B, Kaewkes S, Intapan PM et al (2010) Food-borne trematodiases in Southeast Asia epidemiology, pathology, clinical manifestation and control. Adv Parasitol 72:305–350PubMedGoogle Scholar
  169. 169.
    Watthanakulpanich D, Waikagul J, Maipanich W et al (2010) Haplorchis taichui as a possible etiologic agent of irritable bowel syndrome-like symptoms. Korean J Parasitol 48:225–229PubMedCentralPubMedGoogle Scholar
  170. 170.
    Lee JB, Chi JG, Lee SK et al (1981) Study on the pathology of metagonimiasis in experimentally infected cat intestine. Korean J Parasitol 19:109–129Google Scholar
  171. 171.
    Chi JG, Kim CW, Kim JR et al (1988) Intestinal pathology in human metagonimiasis with ultrastructural observations of parasites. J Korean Med Sci 3:171–177PubMedCentralPubMedGoogle Scholar
  172. 172.
    Sukontason K, Unpunyo P, Sukontason KL et al (2005) Evidence of Haplorchis taichui infection as pathogenic parasite: three case reports. Scand J Infect Dis 37:388–390PubMedGoogle Scholar
  173. 173.
    Cho SY, Kim SI, Kang SY (1987) Specific IgG responses in experimental cat metagonimiasis. Korean J Parasitol 25:149–153Google Scholar
  174. 174.
    El-Ganayni GA, Youssef ME, Handousa AE et al (1989) Serum and intestinal immunoglobulins in heterophyiasis. J Egypt Soc Parasitol 19:219–223PubMedGoogle Scholar
  175. 175.
    Pica R, Castellano C, Cilia C et al (2003) Intestinal fluke infections: the heterophyids. Clin Ther 154:61–63Google Scholar
  176. 176.
    Ditrich O, Kopacek P, Giboda M et al (1991) Serological differentiation of human small fluke infections using Opisthorchis viverrini and Haplorchis taichui antigens. Southeast Asian J Trop Med Public Health 22:174–178PubMedGoogle Scholar
  177. 177.
    Lee SC, Chung YB, Kong Y et al (1993) Antigenic protein fractions of Metagonimus yokogawai reacting with patient sera. Korean J Parasitol 31:43–48PubMedGoogle Scholar
  178. 178.
    Sato M, Pongvongsa T, Sanguankiat S et al (2010) Copro-DNA diagnosis of Opisthorchis viverrini and Haplorchis taichui infection in an endemic area of Lao PDR. Southeast Asian J Trop Med Public Health 41:28–35PubMedGoogle Scholar
  179. 179.
    Wongsawad P, Wongsawad C (2009) Development of PCR-based diagnosis of minute intestinal fluke, Haplorchis taichui. Southeast Asian J Trop Med Public Health 40:919–923PubMedGoogle Scholar
  180. 180.
    Wongsawad C, Wongsawad P, Chuboon S et al (2009) Copro-diagnosis of Haplorchis taichui infection using sedimentation and PCR-based methods. Southeast Asian J Trop Med Public Health 40:924–928PubMedGoogle Scholar
  181. 181.
    Wongsawad C, Wongsawad P, Chai JY et al (2009) Haplorchis taichui, Witenberg, 1930: Development of a HAT-RAPD marker for the detection of minute intestinal fluke infection. Exp Parasitol 123:158–161PubMedGoogle Scholar
  182. 182.
    Van Van K, Dalsgaard A, Blair D et al (2009) Haplorchis pumilio and H. taichui in Vietnam discriminated using ITS-2 DNA sequence data from adults and larvae. Exp Parasitol 123:146–151PubMedGoogle Scholar
  183. 183.
    Thaenkham U, Phuphisut O, Pakdee W et al (2011) Rapid and simple identification of human pathogenic heterophyid intestinal fluke metacercariae by PCR-RFLP. Parasitol Int 60:503–506PubMedGoogle Scholar
  184. 184.
    Jueco NL, Monzon RB (1984) Cathaemasia cabrerai sp.N. (Trematoda: Cathaemasiidae) a new parasite of man in the Philippines. Southeast Asian J Trop Med Public Health 15:427–429PubMedGoogle Scholar
  185. 185.
    Radomyos B, Wongsaroj T, Wilrairatana P et al (1998) Opisthorchiasis and intestinal fluke infections in northern Thailand. Southeast Asian J Trop Med Public Health 29:123–127PubMedGoogle Scholar
  186. 186.
    Kaewkes S, Elkins DB, Haswell-Elkins MR et al (1991) Phaneropsolus spinicirrus n. sp. (Digenea: Lecithodendriidae), a human parasite in Thailand. J Parasitol 77:514–516PubMedGoogle Scholar
  187. 187.
    Eastburn RL, Fritsche TR, Terhune CA (1987) Human intestinal infection with Nanophyetus salmincola from salmonid fishes. Am J Trop Med Hyg 36:586–591PubMedGoogle Scholar
  188. 188.
    Schell SC (1985) Trematodes of North America, north of Mexico. University Press of Idaho, IdahoGoogle Scholar
  189. 189.
    Asada JI, Otagaki H, Morita M et al (1962) A case report on the human infection with Plagiorchis muris Tanabe, 1922 in Japan. Japanese J Parasitol 11:512–516Google Scholar
  190. 190.
    Radomyos P, Bunnag D, Harinasuta C (1989) A new intestinal fluke, Plagiorchis harinasutai, n. sp. Southeast Asian J Trop Med Public Health 20:101–107PubMedGoogle Scholar
  191. 191.
    Hong SJ, Woo HC, Chai JY (1996) A human case of Plagiorchis muris (Tanabe, 1922: Digenea) infection in the Republic of Korea: Freshwater fish as a possible source of infection. J Parasitol 82:647–649PubMedGoogle Scholar
  192. 192.
    Chen CE, Cai GD (1985) Morphological testimony: demonstration of a case of human infestation with Cotylurus japonicus Ishii, 1932 (Trematoda, Strigeidae). Bull Hunan Med Coll 10:31–34Google Scholar
  193. 193.
    Greenberg RM (2005) Are Ca2+ channels targets of praziquantel action? Int J Parasitol 35:1–9PubMedGoogle Scholar
  194. 194.
    Keiser J, Utzinger J (2004) Chemotherapy for major food-borne trematodes: a review. Expert Opin Pharmacother 5:1711–1726PubMedGoogle Scholar
  195. 195.
    Fürst T, Sayasone S, Odermatt P et al (2012) Manifestation, diagnosis, and management of foodborne trematodiasis. Br Med J 26:e4093Google Scholar
  196. 196.
    Keiser J, Utzinger J (2010) The drugs we have and the drugs we need against major helminth infections. Adv Parasitol 73:197–230PubMedGoogle Scholar
  197. 197.
    Toledo R, Bernal MD, Marcilla A (2011) Proteomics of foodborne trematodes. J Proteomics 74:1485–1503PubMedGoogle Scholar
  198. 198.
    Keiser J, Utzinger J (2009) Food-borne trematodiases. Clin Microbiol Rev 22:466–483PubMedCentralPubMedGoogle Scholar
  199. 199.
    Keiser J, Brun R, Fried B et al (2006) Trematocidal activity of praziquantel and artemisinin derivatives: in vitro and in vivo investigations on adult Echinostoma caproni. Antimicrob Agents Chemother 50:803–805PubMedCentralPubMedGoogle Scholar
  200. 200.
    Fathy FM (2011) Anthelmintic effect of artesunate in experimental heterophyiid infection. J Egypt Soc Parasitol 41:469–483PubMedGoogle Scholar
  201. 201.
    Keiser J, Utzinger J, Tanner M et al (2006) The synthetic peroxide OZ78 is effective against Echinostoma caproni and Fasciola hepatica. J Antimicrob Chemother 58:1193–1197PubMedGoogle Scholar
  202. 202.
    Ferreira JFS, Peaden P, Keiser J (2011) In vitro trematocidal effects of crude alcoholic extracts of Artemisia annua, A. absinthium, Asimina triloba, and Fumaria officinalis: trematocidal plant alcoholic extracts. Parasitol Res 109:1585–1592PubMedGoogle Scholar
  203. 203.
    Saxton T, Fried B (2009) An update on metacercarial excystment of trematodes. Parasitol Res 105:1185–1191PubMedGoogle Scholar
  204. 204.
    Wongsawad C, Kawin S, Wongsawad P et al (2005) Some factors affecting Stellantchasmus falcatus metacercaria in laboratory. Southeast Asian J Trop Med Public Health 36:11711–11719Google Scholar
  205. 205.
    Chieffi PP, Gorla MC, Torres DM et al (1992) Human infection by Phagicola sp. (Trematoda, Heterophyidae) in the municipality of Registro, São Paulo State, Brazil. J Trop Med Hyg 95:346–348PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Rafael Toledo
    • 1
  • Carla Muñoz-Antoli
    • 1
  • J. Guillermo Esteban
    • 1
  1. 1.Departamento de Biología Celular y Parasitología, Facultad de FarmaciaUniversidad de ValenciaValenciaSpain

Personalised recommendations